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Different Levels of Hsp70 and Hsc70 Mrna Expression in Iberian Fish Exposed to Distinct River Conditions

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Different Levels of Hsp70 and Hsc70 Mrna Expression in Iberian Fish Exposed to Distinct River Conditions Genetics and Molecular Biology, 36, 1, 61-69 (2013) Copyright © 2013, Sociedade Brasileira de Genética. Printed in Brazil www.sbg.org.br Research Article Different levels of hsp70 and hsc70 mRNA expression in Iberian fish exposed to distinct river conditions Tiago F. Jesus, Ângela Inácio and Maria M. Coelho Centro de Biologia Ambiental, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, Lisbon, Portugal. Abstract Comprehension of the mechanisms by which ectotherms, such as fish, respond to thermal stress is paramount for understanding the threats that environmental changes may pose to wild populations. Heat shock proteins are molec- ular chaperones with an important role in several stress conditions such as high temperatures. In the Iberian Penin- sula, particularly in Portugal, freshwater fish of the genus Squalius are subject to daily and seasonal temperature variations. To examine the extent to which different thermal regimes influence the expression patterns of hsp70 and hsc70 transcripts we exposed two species of Squalius (S. torgalensis and S. carolitertii) to different temperatures (20, 25, 30 and 35 °C). At 35 °C, there was a significant increase in the expression of hsp70 and hsc70 in the south- ern species, S. torgalensis, while the northern species, S. carolitertii, showed no increase in the expression of these genes; however, some individuals of the latter species died when exposed to 35 °C. These results suggest that S. torgalensis may cope better with harsher temperatures that are characteristic of this species natural environment; S. carolitertii, on the other hand, may be unable to deal with the extreme temperatures faced by the southern species. Keywords: Cyprinidae, heat shock proteins, Squalius, thermal stress. Received: June 18, 2012; Accepted: December 14, 2012. Introduction nism has a significant ecological and evolutionary role in Many organisms are frequently exposed to stressful natural populations (Sørensen et al., 2003; Fangue et al., environmental conditions, such as temperature variations, 2006; Straalen and Roelofs, 2006). In addition to thermal that pose substantial challenges to their survival and repro- stress, other factors such as insecticides, heavy metals, des- duction (López-Maury et al., 2008). Stressful conditions iccation, diseases and parasites can also induce Hsp may limit the geographical distribution of organisms by (Lindquist and Craig, 1988; Sørensen et al., 2003; Fangue causing them to move to more suitable locations et al., 2006). Heat shock proteins are vital for proper cell (Hoffmann and Sgrò, 2011). Organisms can also deal with functioning since they facilitate the folding and refolding of stressful conditions by adapting to them, either through proteins and the degradation of misfolded, aggregated or changes in the genetic composition of populations as a re- denaturated proteins (Lindquist and Craig, 1988; Ohtsuka sult of selection, and/or by phenotypic plasticity; without and Suzuki, 2000; Sørensen et al., 2003; Wegele et al., this adaptability many species would become extinct 2004). (Sørensen et al., 2003; Dahlhoff and Rank, 2007; Berg et Several closely related hsp genes have been identi- al., 2010; Hoffmann and Sgrò, 2011). Most animal species fied and grouped into families based on their evolutionary (> 99%), including fish, are ecthoterms that cannot regulate relationships (Lindquist and Craig, 1988). The exten- their body temperature and this ultimately affects their me- sively studied 70-kDa heat shock protein (Hsp70) belongs tabolism (Berg et al., 2010). Since increases in temperature to a multi-gene family and its gene expression varies un- are one of the major consequences of climate change it is der different physiological conditions (Lindquist and important to know how organisms, particularly ecthoterms, Craig, 1988). The genes that encode the Hsp70 proteins respond to high temperatures. (hsp70s) are considered the major hsp gene family and Heat shock proteins (Hsp) are part of an important consist of exclusively inducible (hsps), exclusively con- mechanism that helps organisms to cope with adverse envi- stitutive [Heat shock cognates (hscs)] and even simulta- ronmental conditions such as thermal stress. This mecha- neously inducible and constitutive genes (Lindquist and Craig, 1988; Ohtsuka and Suzuki, 2000; Place and Hofmann, 2001; Sørensen et al., 2003). The hsp70 genes Send correspondence to T.F. Jesus. Faculdade de Ciências, Edifício C2, Room 2.3.12, Universidade de Lisboa, Campo Grande, and the genes that encode the Hsc70 protein (hsc70)be- 1749-016 Lisbon, Portugal. E-mail: [email protected]. long to the hsp70 gene family. Whereas hsp70 genes are 62 Jesus et al. induced by several types of stress, hsc70 genes are mainly constitutively expressed under normal (non-stress) condi- tions (Lindquist and Craig, 1988; Ohtsuka and Suzuki, 2000; Yamashita et al., 2004). Members of the hsp70 gene family have been widely studied in many organisms and distinct expression patterns have been found. Several studies have reported a relation- ship between the expression patterns of hsp70 and environ- mental variations throughout a species range (Sørensen et al., 2001; Fangue et al., 2006; Karl et al., 2009; Sørensen et al., 2009; Blackman, 2010; Sarup and Loeschcke, 2010). For example, Fangue et al. (2006) detected significant dif- ferences in the gene expression levels of hsp70 between northern and southern populations of Fundulus heteroclitus in North America, with the latter being exposed to higher temperatures. Similarly, Sørensen et al. (2009) found that southern populations of Rana temporaria from Sweden, when exposed to higher temperatures, had the highest lev- Figure 1 - Geographical distribution of S. torgalensis and S. carolitertii in els of Hsp70 protein expression. Portugal, with the respective sampling sites marked with triangles. The hsc70 gene was initially described as being con- stitutively expressed under normal and stressful conditions The main goal of this study was to gain insights into (Lindquist and Craig, 1988; Place and Hofmann, 2001; Yeh the potentially important molecular mechanism involved in and Hsu, 2002; Yamashita et al., 2004). Fangue et al. the response of S. carolitertii and S. torgalensis to thermal (2006) reported that individuals from southern populations stress, particularly since these species inhabit regions with of F. heteroclitus showed enhanced expression of this gene distinct environmental regimes. Specifically, we examined at higher temperatures. This finding demonstrates the im- the hsp70 and hsc70 gene transcription patterns for each portance of studying the expression of hsp70 genes in species exposed to different temperatures and compared the closely related species or populations exposed to different patterns between the two species; we also tried to correlate temperature regimes in their natural habitats. These find- our findings with the ecological context of each species. ings also suggest that Hsps play an important role in ther- Finally, we examined whether the patterns of transcript ex- mal tolerance and that, despite being occasionally parado- pression (for the genes of interest) were similar to those of xical, the expression patterns of these genes must be muscle, which is the most frequently used tissue in such interpreted according to the ecological context of each spe- studies (Yamashita et al., 2004). The results described here cies (Sørensen et al., 2003). provide useful insights into the roles of hsp70 and hsc70 In the Iberian Peninsula, particularly in Portugal, the gene expression in the response of Iberian Squalius to ther- congeneric freshwater fish species, Squalius carolitertii mal stress. (Cyprinidae) (Doadrio, 1988), a species of least concern (Rogado et al., 2006), and Squalius torgalensis (Coelho et Methods al., 1998), a critically endangered species (Cabral et al., 2006), inhabit distinct regions. Squalius carolitertii inhab- Sampling and maintenance of fish its the northern region whereas S. torgalensis is restricted to a small river basin (the Mira river) in the southwestern re- Adult fish (6-8 cm long) of S. carolitertii and S. gion (Figure 1) (Cabral et al., 2006). In these areas, the two torgalensis were collected from Portuguese rivers by elec- species are exposed to different environmental conditions tro-fishing (300 V, 4 A) (Figure 1). The pulses used were of with distinct seasonal and even daily water temperature low duration to avoid killing juveniles. Sampling was done variations. The northern rivers of Portugal have lower tem- during the spring, when the water temperature in the south- peratures and fewer temperature fluctuations than the ern and northern rivers is ~18-22 °C. Fish of both sexes southern rivers (Henriques et al., 2010; SNIRH). In north- were used since there is no sexual dimorphism in either spe- ern rivers, the maximum temperature usually does not ex- cies. Squalius torgalensis individuals were sampled in the ceed 31 °C (range: 3-31 °C), whereas southern rivers are Mira river basin since this species is endemic to this region characterized by an intermittent regime of floods and and individuals of S. carolitertii were collected in the Mon- droughts in which, during the dry season, freshwater fish dego, Vouga and Douro river basins of the northern region. are trapped in small pools in which temperatures can reach The fish were maintained in ~30 L aquaria at 20 °C (mean 38 °C (range: 4-38 °C) (Magalhães et al., 2003; Henriques temperature observed during
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